Increased mitochondrial uncoupling proteins, respiratory uncoupling and decreased efficiency in the chronically infarcted rat heart

Journal of Molecular and Cellular Cardiology

Volumn 44, Issue 4, 2008, Pages 694-700

  Murray, Andrew J ^a   Cole, Mark A ^a   Lygate, Craig A ^b   Carr, Carolyn A ^a   Stuckey, Daniel J ^a   Little, Sarah E ^a   Neubauer, Stefan ^b   Clarke, Kieran ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Department of Cardiovascular Medicine ^*  (United Kingdom)

Author keywords

Cardiac efficiency; Energy metabolism; Fatty acid metabolism; Heart failure; Mitochondria

Indexed keywords

FATTY ACID; MITOCHONDRIAL PROTEIN; PALMITIC ACID; UNCOUPLING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROL GROUP; CONTROLLED STUDY; ENERGY TRANSFER; FATTY ACID BLOOD LEVEL; HEART EJECTION FRACTION; HEART INFARCTION; HEART MUSCLE; MALE; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STATISTICAL SIGNIFICANCE;

ADENOSINE DIPHOSPHATE; ANIMALS; CARDIAC OUTPUT; CELL RESPIRATION; CITRATE (SI)-SYNTHASE; CORONARY CIRCULATION; HEART FAILURE; ION CHANNELS; MALE; MITOCHONDRIA, HEART; MITOCHONDRIAL PROTEINS; MYOCARDIAL INFARCTION; OXYGEN CONSUMPTION; PERFUSION; RATS; RATS, WISTAR;

RATTUS;

EID: 42749085693     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2008.01.008     Document Type: Article

References (41)

1. Paolisso G., Gambardella A., Galzerano D., D'Amore A., Rubino P., Verza M., et al. Total-body and myocardial substrate oxidation in congestive heart failure. Metabolism 43 (1994) 174-179
2. Neubauer S., Horn M., Cramer M., Harre K., Newell J.B., Peters W., et al. Myocardial phosphocreatine-to-ATP ratio is a predictor of mortality in patients with dilated cardiomyopathy. Circulation 96 (1997) 2190-2196
3. Neubauer S., Horn M., Naumann A., Tian R., Hu K., Laser M., et al. Impairment of energy metabolism in intact residual myocardium of rat hearts with chronic myocardial infarction. J Clin Invest 95 (1995) 1092-1100
4. Murray A.J., Lygate C.A., Cole M.A., Carr C.A., Radda G.K., Neubauer S., et al. Insulin resistance, abnormal energy metabolism and increased ischemic damage in the chronically infarcted rat heart. Cardiovasc Res 71 (2006) 149-157
5. Scheuermann-Freestone M., Madsen P.L., Manners D., Blamire A.M., Buckingham R.E., Styles P., et al. Abnormal cardiac and skeletal muscle energy metabolism in patients with type 2 diabetes. Circulation 107 (2003) 3040-3046
6. van Bilsen M., van der Vusse G.J., and Reneman R.S. Transcriptional regulation of metabolic processes: implications for cardiac metabolism. Eur J Physiol 437 (1998) 2-14
7. Gilde A.J., van der Lee K.A.J.M., Willemsen P.H.M., Chinetti G., van der Leij F.R., van der Vusse G.J., et al. Peroxisome proliferator-activated receptor (PPAR) alpha and PPAR beta/delta, but not PPAR gamma, modulate the expression of genes involved in cardiac lipid metabolism. Circ Res 92 (2003) 518-524
8. Vettor R., Fabris R., Serra R., Lombardi A.M., Tonello C., Granzotto M., et al. Changes in FAT/CD36, UCP2, UCP3 and GLUT4 gene expression during lipid infusion in rat skeletal and heart muscle. Int J Obes Relat Metab Disord 26 (2002) 838-847
9. Murray A.J., Anderson R.E., Watson G.C., Radda G.K., and Clarke K. Uncoupling proteins in human heart. Lancet 364 (2004) 1786-1788
10. Ray J., Noll F., Daut J., and Hanley P.J. Long-chain fatty acids increase basal metabolism and depolarize mitochondria in cardiac muscle cells. Am J Heart Circ Physiol 282 (2002) H1495-H1501
11. Boehm E.A., Jones B.E., Radda G.K., Veech R.L., and Clarke K. Increased uncoupling proteins and decreased cardiac efficiency in the palmitate-perfused hyperthyroid rat heart. Am J Physiol 280 (2001) H977-H983
12. Lygate C.A., Hulbert K., Monfared M., Cole M.A., Clarke K., and Neubauer S. The PPARgamma-activator rosiglitazone does not alter remodeling but increases mortality in rats post-myocardial infarction. Cardiovasc Res 58 (2003) 632-637
13. Palmer J.W., Tandler B., and Hoppel C.L. Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J Biol Chem 252 (1977) 8731-8739
14. Kerner J., Turkaly P.J., Minkler P.E., and Hoppel C.L. Aging skeletal muscle mitochondria in the rat: decreased uncoupling protein-3 content. Am J Physiol Endocrinol Metab 281 (2001) E1054-E1062
15. Estabrook R.W. Mitochondrial respiratory control and polarographic measurement of ADP/O ratios. Methods Enzymol 10 (1967) 41-47
16. Murray A.J., Panagia M., Hauton D., Gibbons G.F., and Clarke K. Plasma free fatty acids and peroxisome proliferator-activated receptor alpha in the control of myocardial uncoupling protein levels. Diabetes 54 (2005) 3496-3502
17. Srere P.A. Citrate synthase. Methods Enzymol 13 (1969) 3-11
18. Sato K., Kashiwaya Y., Keon C.A., Tsuchiya N., King M.T., Radda G.K., et al. Insulin, ketone bodies, and mitochondrial energy transduction. Faseb J 9 (1995) 651-658
19. Pool P.E., Spann Jr. J.F., Buccino R.A., Sonnenblick E.H., and Braunwald E. Myocardial high energy phosphate stores in cardiac hypertrophy and heart failure. Circ Res 21 (1967) 365-373
20. Katz A.M. The myocardium in congestive heart failure. Am J Cardiol 63 (1989) 12A-16A
21. Sanbe A., Tanonaka K., Kobayasi R., and Takeo S. Effects of long-term therapy with ACE inhibitors, captopril, enalapril and trandolapril on myocardial energy metabolism in rats with heart failure following myocardial infarction. J Mol Cell Cardiol 27 (1995) 2209-2222
22. Horn M., Remkes H., Stromer H., Dienesch C., and Neubauer S. Chronic phosphocreatine depletion by the creatine analogue beta-guanidinopropionate is associated with increased mortality and loss of ATP in rats after myocardial infarction. Circulation 104 (2001) 1844-1849
23. Heather L.C., Cole M.A., Lygate C.A., Evans R.D., Stuckey D.J., Murray A.J., et al. Fatty acid transporter levels and palmitate oxidation rate correlate with ejection fraction in the infarcted rat heart. Cardiovasc Res 72 (2006) 430-437
24. Krauss S., Zhang C.-Y., and Lowell B.B. A significant portion of mitochondrial proton leak in intact thymocytes depends on expression of UCP2. PNAS 99 (2002) 118-122
25. Cline G.W., Vidal-Puig A.J., Dufour S., Cadman K.S., Lowell B.B., and Shulman G.I. In vivo effects of uncoupling protein-3 gene disruption on mitochondrial energy metabolism. J Biol Chem 276 (2001) 20240-20244
26. Clarke K., Sunn N., and Willis R.J. 31P NMR spectroscopy of hypertrophied rat heart: effect of graded global ischemia. J Mol Cell Cardiol 21 (1989) 1315-1325
27. van Bilsen M., van der Vusse G.J., Gilde A.J., Lindhout M., and van der Lee K.A.J.M. Peroxisome proliferator-activated receptors: lipid binding proteins controlling gene expression. Mol Cell Biochem 239 (2002) 131-138
28. Samec S., Seydoux J., and Dulloo A.G. Post-starvation gene expression of skeletal muscle uncoupling protein 2 and uncoupling protein 3 in response to dietary fat levels and fatty acid composition. Diabetes 48 (1999) 436-441
29. Armstrong M.B., and Towle H.C. Polyunsaturated fatty acids stimulate hepatic UCP-2 expression via a PPARa-mediated pathway. Am J Physiol Endocrinol Metab 281 (2001) E1197-E1204
30. Rodriguez A.M., Portillo M.P., Pico C., Macarulla M.T., and Palou A. Olive oil feeding up-regulates uncoupling protein genes in rat brown adipose tissue and skeletal muscle. Am J Clin Nutr 75 (2002) 213-220
31. Samec S., Seydoux J., and Dulloo A.G. Interorgan signaling between adipose tissue metabolism and skeletal muscle uncoupling protein homologs. Is there a role for circulating free fatty acids?. Diabetes 47 (1998) 1693-1698
32. Ide T., Tsutsui H., Hayashidani S., Kang D., Suematsu N., Nakamura K., et al. Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circ Res 88 (2001) 529-535
33. Essop M.F., Razeghi P., McLeod C., Young M.E., Taegtmeyer H., and Sack M.N. Hypoxia-induced decrease of UCP3 gene expression in rat heart parallels metabolic gene switching but fails to affect mitochondrial respiratory coupling. Biochem Biophys Res Commun 314 (2004) 561-564
34. Cadenas S., Buckingham J.A., Samec S., Seydoux J., Din N., Dulloo A.G., et al. UCP2 and UCP3 rise in starved rat skeletal muscle but mitochondrial proton conductance is unchanged. FEBS Lett 462 (1999) 257-260
35. Cadenas S., Echtay K.S., Harper J.A., Jekabsons M.B., Buckingham J.A., Grau E., et al. The basal proton conductance of skeletal muscle mitochondria from transgenic mice overexpressing or lacking uncoupling protein-3. J Biol Chem 277 (2002) 2773-2778
36. Sivitz W.I., Fink B.D., and Donohoue P.A. Fasting and leptin modulate adipose and muscle uncoupling protein: divergent effects between messenger ribonucleic acid and protein expression. Endocrinology 140 (1999) 1511-1519
37. Jaburek M., Varecha M., Gimeno R.E., Dembski M., Jezek P., Zhang M., et al. Transport function and regulation of mitochondrial uncoupling proteins 2 and 3. J Biol Chem 274 (1999) 26003-26007
38. McFalls E.O., Sluiter W., Schoonderwoerd K., Manintveld O.C., Lamers J.M., Bezstarosti K., et al. Mitochondrial adaptations within chronically ischemic swine myocardium. J Mol Cell Cardiol 41 (2006) 980-988
39. Echtay K.S., Roussel D., St-Pierre J., Jekabsons M.B., Cadenas S., Stuart J.A., et al. Superoxide activates mitochondrial uncoupling proteins. Nature 415 (2002) 96-99
40. Schrauwen P., Hoeks J., Schaart G., Kornips E., Binas B., van de Vusse G.J., et al. Uncoupling protein 3 as a mitochondrial fatty acid anion exporter. FASEB J 17 (2003) 2272-2274
41. Esposito G., Petrotta M.P., Perrino G., Guerriero R., Sorda G., Borgia F., et al. Cardioprotective role of the uncoupling protein 3 following chronic catecholamine administration. Circulation 116 (2007) II-91 [Suppl]